The spatial and temporal variation in the availability of suitable habitat within metapopulations determines colonization-extinction events, regulates local population sizes and eventually affects local population and metapopulation stability. Insights into the impact of such a spatiotemporal variation on the local population and metapopulation dynamics are principally derived from classical metapopulation theory and have not been experimentally validated. By manipulating spatial structure in artificial metapopulations of the spider mite Tetranychus urticae, we test to which degree spatial (mainland-island metapopulations) and spatiotemporal variation (classical metapopulations) in habitat availability affects the dynamics of the metapopulations relative to systems where habitat is constantly available in time and space (patchy metapopulations). Our experiment demonstrates that (i) spatial variation in habitat availability decreases variance in metapopulation size and decreases density-dependent dispersal at the metapopulation level, while (ii) spatiotemporal variation in habitat availability increases patch extinction rates, decreases local population and metapopulation sizes and decreases density dependence in population growth rates. We found dispersal to be negatively density dependent and overall low in the spatial variable mainland-island metapopulation. This demographic variation subsequently impacts local and regional population dynamics and determines patterns of metapopulation stability. Both local and metapopulation-level variabilities are minimized in mainland-island metapopulations relative to classical and patchy ones.

Abstract. Dispersal is essential for population persistence in transient environments. While costs of dispersal are ubiquitous, individual advantages of dispersal remain poorly understood. Not all individuals from a population disperse, and individual heterogeneity in costs and benefits of dispersal underlie phenotype-dependent dispersal strategies. Dispersing phenotypes are always expected to maximize their fitness by adaptive decision making relative to the alternative strategy of remaining philopatric. While this first principle is well acknowledged in theoretical ecology, empirical verification is extremely difficult, due to a plethora of experimental constraints. We studied fitness prospects of dispersal in a game theoretical context using the two-spotted spider mite Tetranychus urticae as a model species. We demonstrate that dispersing phenotypes represent those individuals able to maximize their fitness in a novel, less populated environment reached after dispersal. In contrast to philopatric phenotypes, successful dispersers performed better in a low density post-dispersal context, but worse in a high density philopatric context. They increased fitness about 450% relative to the strategy of remaining philopatric. The optimization of phenotype-dependent dispersal, thus, maximizes fitness.

BackgroundSoil biota may trigger strong physiological responses in plants and consequently induce distinct phenotypes. Plant phenotype, in turn, has a strong impact on herbivore performance. Here, we tested the hypothesis that aboveground herbivores are able to adapt to plant phenotypes induced by soil biota.Methodology and Principal FindingsWe bred spider mites for 15 generations on snap beans with three different belowground biotic interactions: (i) no biota (to serve as control), (ii) arbuscular mycorrhizal fungi and (ii) root-feeding nematodes. Subsequently, we conducted a reciprocal selection experiment using these spider mites, which had been kept on the differently treated plants. Belowground treatments induced changes in plant biomass, nutrient composition and water content. No direct chemical defence through cyanogenesis was detected in any of the plant groups. Growth rates of spider mites were higher on the ecotypes on which they were bred for 15 generations, although the statistical significance disappeared for mites from the nematode treatment when corrected for all multiple comparisons.Conclusion/SignificanceThese results demonstrate that belowground biota may indeed impose selection on the aboveground insect herbivores mediated by the host plant. The observed adaptation was driven by variable quantitative changes of the different separately studied life history traits (i.e. fecundity, longevity, sex-ratio, time to maturity).

International audienceThe persistence and dynamics of populations largely depend on the way they are configured and integrated into space and the ensuing eco-evolutionary dynamics. * We manipulated spatial and temporal variation in patch size in replicated experimental metapopulations of the herbivore mite Tetranychus urticae and followed evolutionary dynamics over approximately 30 generations. * A significant divergence in life-history traits, physiological endpoints and gene expression was recorded in the spatially and spatiotemporally variable metapopulation, but also a remarkable convergence relative to the stable reference metapopulation in traits related to size and fecundity and in its transcriptional regulation. * The observed evolutionary dynamics are tightly linked to demographic changes, more specifically frequent episodes of resource shortage that increased the reproductive performance of mites on tomato, a challenging host plant. This points towards a general, adaptive stress response in stable spatial variable and spatiotemporal variable metapopulations that pre-adapts a herbivore arthropod to novel environmental stressor

The persistence and dynamics of populations largely depends on the way they are configured and integrated into space and the ensuing eco-evolutionary dynamics. We manipulated spatial and temporal variation in patch size in replicated experimental metapopulations of the herbivore mite Tetranychus urticae. Evolution over approximately 30 generations in the spatially and spatiotemporally variable metapopulations induced a significant divergence in life history traits, physiological endpoints and gene expression, but also a remarkable convergence relative to the stable reference patchy metapopulation in traits related to size and fecundity and in its transcriptional regulation. The observed evolutionary dynamics are tightly linked to demographic changes, more specifically frequent episodes of resource shortage, and increased the reproductive performance of mites on tomato, a challenging host plant. This points towards a general, adaptive stress response in stable spatial variable and spatiotemporal variable metapopulations that pre-adapts a herbivore arthropod to novel environmental stressors.